Determinants of host species range in plant viruses Free

Abstract

Prediction of pathogen emergence is an important field of research, both in human health and in agronomy. Most studies of pathogen emergence have focused on the ecological or anthropic factors involved rather than on the role of intrinsic pathogen properties. The capacity of pathogens to infect a large set of host species, i.e. to possess a large host range breadth (HRB), is tightly linked to their emergence propensity. Using an extensive plant virus database, we found that four traits related to virus genome or transmission properties were strongly and robustly linked to virus HRB. Broader host ranges were observed for viruses with single-stranded genomes, those with three genome segments and nematode-transmitted viruses. Also, two contrasted groups of seed-transmitted viruses were evidenced. Those with a single-stranded genome had larger HRB than non-seed-transmitted viruses, whereas those with a double-stranded genome (almost exclusively RNA) had an extremely small HRB. From the plant side, the family taxonomic rank appeared as a critical threshold for virus host range, with a highly significant increase in barriers to infection between plant families. Accordingly, the plant–virus infectivity matrix shows a dual structure pattern: a modular pattern mainly due to viruses specialized to infect plants of a given family and a nested pattern due to generalist viruses. These results contribute to a better prediction of virus host jumps and emergence risks.

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2017-04-01
2024-03-28
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References

  1. Woolhouse MEJ, Haydon DT, Antia R. Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 2005; 20:238–244 [View Article][PubMed]
    [Google Scholar]
  2. Schrag SJ, Wiener P. Emerging infectious disease: what are the relative roles of ecology and evolution?. Trends Ecol Evol 1995; 10:319–324 [View Article][PubMed]
    [Google Scholar]
  3. Pulliam JRC. Viral host jumps: moving toward a predictive framework. Ecohealth 2008; 5:80–91 [View Article][PubMed]
    [Google Scholar]
  4. Dijskra J. Importance of host ranges and other biological properties for the taxonomy of plant viruses. Arch Virol 1992; 5:173–176 [Crossref]
    [Google Scholar]
  5. Suehiro N, Natsuaki T, Watanabe T, Okuda S. An important determinant of the ability of Turnip mosaic virus to infect Brassica spp. and/or Raphanus sativus is in its P3 protein. J Gen Virol 2004; 85:2087–2098 [View Article][PubMed]
    [Google Scholar]
  6. Chen KC, Chiang CH, Raja JA, Liu FL, Tai CH et al. A single amino acid of niapro of Papaya ringspot virus determines host specificity for infection of papaya. Mol Plant Microbe Interact 2008; 21:1046–1057 [View Article][PubMed]
    [Google Scholar]
  7. Tatineni S, Robertson CJ, Garnsey SM, Dawson WO. A plant virus evolved by acquiring multiple nonconserved genes to extend its host range. Proc Natl Acad Sci USA 2011; 108:17366–17371 [View Article][PubMed]
    [Google Scholar]
  8. Poulicard N, Pinel-Galzi A, Traoré O, Vignols F, Ghesquière A et al. Historical contingencies modulate the adaptability of Rice yellow mottle virus . PLoS Pathog 2012; 8:e1002482 [View Article][PubMed]
    [Google Scholar]
  9. Vassilakos N, Simon V, Tzima A, Johansen E, Moury B. Genetic determinism and evolutionary reconstruction of a host jump in a plant virus. Mol Biol Evol 2016; 33:541–553 [View Article][PubMed]
    [Google Scholar]
  10. Gibbs A. Evolution and origins of tobamoviruses. Philos Trans R Soc Lond B Biol Sci 1999; 354:593–602 [View Article][PubMed]
    [Google Scholar]
  11. Wu B, Melcher U, Guo X, Wang X, Fan L et al. Assessment of codivergence of Mastreviruses with their plant hosts. BMC Evol Biol 2008; 8:335 [View Article][PubMed]
    [Google Scholar]
  12. Woolhouse MEJ, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis 2005; 11:1842–1847 [View Article][PubMed]
    [Google Scholar]
  13. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR et al. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 2004; 19:535–544 [View Article][PubMed]
    [Google Scholar]
  14. Jones RAC. Plant virus emergence and evolution: origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res 2009; 141:113–130 [View Article][PubMed]
    [Google Scholar]
  15. Brunt AA, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L et al. Plant Viruses Online: Descriptions and Lists from the VIDE Database Version: 20th August 1996 http://sdb.im.ac.cn/vide/refs.htm 1996
    [Google Scholar]
  16. Hill MO. Diversity and evenness: a unifying notation and its consequences. Ecology 1973; 54:427–432 [View Article]
    [Google Scholar]
  17. Power AG, Flecker AS. Virus specificity in disease systems: are species redundant?. In Kareiva P, Levin SA. (editors) The Importance of Species: Perspectives on Expendability and Triage Princeton, USA: Princeton University Press; 2003 pp. 330–347
    [Google Scholar]
  18. Weitz JS, Poisot T, Meyer JR, Flores CO, Valverde S et al. Phage–bacteria infection networks. Trends Microbiol 2013; 21:82–91 [View Article][PubMed]
    [Google Scholar]
  19. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses London, UK, Waltham, MA and San Diego, CA, USA: Elsevier Academic Press; 2012
    [Google Scholar]
  20. Desbiez C, Moury B, Lecoq H. The hallmarks of ‘green’ viruses: do plant viruses evolve differently from the others?. Inf Genet Evol 2011; 11:812–824 [View Article]
    [Google Scholar]
  21. Gilbert GS, Magarey R, Suiter K, Webb CO. Evolutionary tools for phytosanitary risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens. Evol Appl 2012; 5:869–878 [View Article][PubMed]
    [Google Scholar]
  22. Vacher C, Piou D, Desprez-Loustau M-L. Architecture of an antagonistic tree/fungus network: the asymmetric influence of past evolutionary history. PLoS One 2008; 3:e1740 [View Article]
    [Google Scholar]
  23. Sanjuán R. From molecular genetics to phylodynamics: evolutionary relevance of mutation rates across viruses. PLoS Pathog 2012; 8:e1002685 [View Article][PubMed]
    [Google Scholar]
  24. Frederico LA, Kunkel TA, Shaw BR. A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry 1990; 29:2532–2537 [View Article][PubMed]
    [Google Scholar]
  25. Sicard A, Michalakis Y, Gutiérrez S, Blanc S. The strange lifestyle of multipartite viruses. PLoS Pathog 2016; 12:e1005819 [View Article][PubMed]
    [Google Scholar]
  26. Nee S. The evolution of multicompartmental genomes in viruses. J Mol Evol 1987; 25:277–281 [View Article][PubMed]
    [Google Scholar]
  27. Chao L. Levels of selection, evolution of sex in RNA viruses, and the origin of life. J Theor Biol 1991; 153:229–246 [Crossref]
    [Google Scholar]
  28. Ojosnegros S, García-Arriaza J, Escarmís C, Manrubia SC, Perales C et al. Viral genome segmentation can result from a trade-off between genetic content and particle stability. PLoS Genet 2011; 7:e1001344 [View Article][PubMed]
    [Google Scholar]
  29. Sicard A, Yvon M, Timchenko T, Gronenborn B, Michalakis Y et al. Gene copy number is differentially regulated in a multipartite virus. Nat Commun 2013; 4:2248 [View Article]
    [Google Scholar]
  30. Maynard Smith J. The Evolution of Sex Cambridge, UK: Cambridge University Press; 1978
    [Google Scholar]
  31. Gutiérrez S, Michalakis Y, Blanc S. Virus population bottlenecks during within-host progression and host-to-host transmission. Curr Opin Virol 2012; 2:546–555 [View Article][PubMed]
    [Google Scholar]
  32. Tromas N, Zwart MP, Lafforgue G, Elena SF. Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLoS Genet 2014; 10:e1004186 [View Article][PubMed]
    [Google Scholar]
  33. Iranzo J, Manrubia SC. Evolutionary dynamics of genome segmentation in multipartite viruses. Proc Biol Sci 2012; 279:3812–3819 [View Article][PubMed]
    [Google Scholar]
  34. Stewart AD, Logsdon JM, Kelley SE. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 2005; 59:730–739 [View Article][PubMed]
    [Google Scholar]
  35. Taylor CE, Brown DJF, Neilson R, Jones AT. The persistence and spread of Xiphinema diversicaudatum in cultivated and uncultivated biotopes. Ann Appl Biol 1994; 124:469–477 [View Article]
    [Google Scholar]
  36. De La Cruz A, López L, Tenllado F, Díaz-Ruíz JR, Sanz AI et al. The coat protein is required for the elicitation of the Capsicum L2 gene-mediated resistance against the tobamoviruses. Mol Plant Microbe Interact 1997; 10:107–113 [View Article][PubMed]
    [Google Scholar]
  37. Tomita R, Sekine KT, Mizumoto H, Sakamoto M, Murai J et al. Genetic basis for the hierarchical interaction between Tobamovirus spp. and L resistance gene alleles from different pepper species. Mol Plant Microbe Interact 2011; 24:108–117 [View Article][PubMed]
    [Google Scholar]
  38. Andersen K, Johansen IE. A single conserved amino acid in the coat protein gene of pea seed-borne mosaic Potyvirus modulates the ability of the virus to move systemically in Chenopodium quinoa . Virology 1998; 241:304–311 [View Article][PubMed]
    [Google Scholar]
  39. Sekine KT, Ishihara T, Hase S, Kusano T, Shah J et al. Single amino acid alterations in Arabidopsis thaliana RCY1 compromise resistance to Cucumber mosaic virus, but differentially suppress hypersensitive response-like cell death. Plant Mol Biol 2006; 62:669–682 [View Article][PubMed]
    [Google Scholar]
  40. Desbiez C, Chandeysson C, Lecoq H. A short motif in the N-terminal part of the coat protein is a host-specific determinant of systemic infectivity for two potyviruses. Mol Plant Pathol 2014; 15:217–221 [View Article][PubMed]
    [Google Scholar]
  41. Garcı́a-Castillo S, Marcos JF, Pallás V, Sánchez-Pina MA. Influence of the plant growing conditions on the translocation routes and systemic infection of carnation mottle virus in Chenopodium quinoa plants. Physiol Mol Plant Pathol 2001; 58:229–238 [View Article]
    [Google Scholar]
  42. R Core Team 2013; R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. www.R-project.org/
  43. Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH et al. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 2014; 84:45–67 [View Article]
    [Google Scholar]
  44. Watson L, Dallwitz MJ. The families of angiosperms: automated descriptions, with interactive identification and information retrieval. Austral Syst Bot 1991; 4:681–695 [View Article]
    [Google Scholar]
  45. Watson L, Dallwitz MJ. 1992; The families of flowering plants: descriptions, illustrations, identification and information retrieval. ftp://www.keil.ukans.edu/pub/delta/
  46. Stevens PF. 2012; Angiosperm phylogeny website version 12, July 2012. www.mobot.org/MOBOT/research/APweb/
  47. Flores CO, Valverde S, Weitz JS. Multi-scale structure and geographic drivers of cross-infection within marine bacteria and phages. Isme J 2013; 7:520–532 [View Article][PubMed]
    [Google Scholar]
  48. Moury B, Janzac B, Ruellan Y, Simon V, Ben Khalifa M et al. Interaction patterns between Potato virus Y and eIF4E-mediated recessive resistance in the Solanaceae . J Virol 2014; 88:9799–9807 [View Article][PubMed]
    [Google Scholar]
  49. Hillung J, Cuevas JM, Valverde S, Elena SF. Experimental evolution of an emerging plant virus in host genotypes that differ in their susceptibility to infection. Evolution 2014; 68:2467–2480 [View Article][PubMed]
    [Google Scholar]
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